Guyanagarika, a new ectomycorrhizal genus of Agaricales from the Neotropics Marisol S ANCHEZ-GARC IA a, * ,1 , Terry W. HENKEL b , Mary Catherine AIME c , Matthew E. SMITH d , Patrick Brandon MATHENY a a Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN 37996, USA b Department of Biological Sciences, Humboldt State University, Arcata, CA 95521, USA c Department of Botany & Plant Pathology, Purdue University, West Lafayette, IN 47907, USA d Department of Plant Pathology, University of Florida, Gainesville, FL 32611, USA article info Article history: Received 6 June 2016 Received in revised form 29 July 2016 Accepted 9 August 2016 Available online 20 August 2016 Corresponding Editor: Ursula Peintner Keywords: Basidiomycota Cryptic species Dicymbe Fungal diversity Systematics abstract A new genus and three new species of Agaricales are described from the Pakaraima Moun- tains of Guyana in the central Guiana Shield. All three of these new species fruit on the ground in association with species of the ectomycorrhizal (ECM) tree genus Dicymbe (Faba- ceae subfam. Caesalpinioideae) and one species has been shown to form ectomycorrhizas. Multi-locus molecular phylogenetic analyses place Guyanagarika gen. nov. within the Cata- thelasma clade, a lineage in the suborder Tricholomatineae of the Agaricales. We formally recognize this ‘Catathelasma clade’ as an expanded family Catathelasmataceae that in- cludes the genera Callistosporium, Catathelasma, Guyanagarika, Macrocybe, Pleurocollybia, and Pseudolaccaria. Within the Catathelasmataceae, Catathelasma and Guyanagarika repre- sent independent origins of the ectomycorrhizal habit. Guyanagarika is the first docu- mented case of an ECM Agaricales genus known only from the Neotropics. ª 2016 British Mycological Society. Published by Elsevier Ltd. All rights reserved. Introduction Fungi represent one of the most diverse groups of organisms with an estimated 5.1 million species, the great majority of which remain to be discovered (O’Brien et al. 2005; Blackwell 2011). In addition to their great taxonomic diversity, fungi play vital roles in nutrient cycling processes in terrestrial eco- systems through decomposition of organic matter, forming mycorrhizal symbioses, and as parasites (Leake & Read 1997). Traditionally, fungal species have been recognized based on micro- and macromorphological characters (e.g. Singer & Smith 1943; Singer 1955; Halling 1992; Manimohan et al. 1995; Adamc ık & Buyck 2011). However, the use of morphology to establish species boundaries may often be inadequate. This is mainly because most of the phenotypic characters used to identify species are based on the sporocarps, which represent a single and short part of the fungal life cycle and have a pau- city of measurable characters relative to most other organ- isms (Petersen & Hughes 1999). The use of other criteria such as interbreeding potential (e.g. Ota et al. 1998; Aanen & Kuyper 1999), or phylogenetic concordance of multiple genes to indicate evolutionary independence of lineages has enabled * Corresponding author. Tel.: þ1 508 793 7622; fax: þ1 508 793 7174. E-mail address: [email protected](M. Sanchez-Garc ıa). 1 Present address: Biology Department, Clark University, Worcester, MA 01610, USA. journal homepage: www.elsevier.com/locate/funbio fungal biology 120 (2016) 1540 e1553 http://dx.doi.org/10.1016/j.funbio.2016.08.005 1878-6146/ª 2016 British Mycological Society. Published by Elsevier Ltd. All rights reserved.
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journa l homepage : www.e lsev ier . com/ loca te / funb io
Guyanagarika, a new ectomycorrhizal genus ofAgaricales from the Neotropics
Marisol S �ANCHEZ-GARC�IAa,*,1, Terry W. HENKELb, Mary Catherine AIMEc,Matthew E. SMITHd, Patrick Brandon MATHENYa
aDepartment of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN 37996, USAbDepartment of Biological Sciences, Humboldt State University, Arcata, CA 95521, USAcDepartment of Botany & Plant Pathology, Purdue University, West Lafayette, IN 47907, USAdDepartment of Plant Pathology, University of Florida, Gainesville, FL 32611, USA
cybe, and Clitocybe aff. fellea. While there are no obvious
morphological or ecological synapomorphies uniting mem-
bers of the Catathelasmataceae (Table 1), in previous studies
these taxa have consistently formed a monophyletic group
within the suborder Tricholomatineae (Matheny et al. 2006;
Ammirati et al. 2007; S�anchez-Garc�ıa et al. 2014). Guyanagarika
is strongly supported as a sister taxon to these taxa within the
expanded Catathelasmataceae (Fig 1).
The relationship between Cleistocybe and Catathelasma has
been examined in detail by Ammirati et al. (2007); both genera
are characterized by having a partial veil, divergent hymeno-
phoral trama, and acyanophilic spores. Based on these mor-
phological similarities, and the fact that the phylogenetic
position of Cleistocybe within the Tricholomatineae is not
well supported (Fig 1), we consider that this taxon may cer-
tainly be part of the Catathelasmataceae, and that failure to
recover Cleistocybe as part of this family could be due to miss-
ing data (the lack of rpb1 and rpb2 sequences) in our
A new ectomycorrhizal genus of Agaricales from the Neotropics 1551
phylogenetic analyses. These two loci have been shown to in-
crease resolution and have higher proportions of informative
characters than ribosomal DNA sequences (Matheny et al.
2002; Frøslev et al. 2005; Schoch et al. 2009); however, to date
only ribosomal sequences are available for Cleistocybe. Addi-
tionally, based on our phylogenetic analyses Clitocybe fellea ap-
pears congeneric with Pseudolaccaria, although future work is
needed to determine whether it is conspecific or a distinct
species of Pseudolaccaria, as has been previously discussed by
Lavorato et al. (2015).
Guyanagarika represents an independent evolutionary ori-
gin of the ECM lifestyle within the Catathelasmataceae, and
within the Agaricales in general. While some putatively en-
demic ECM lineages have been detected from ECM root se-
quences from various tropical sites (Tedersoo & Smith 2013)
and some unique ECM Neotropical genera in the Boletaceae
have recently been described (Smith et al. 2015; Henkel et al.
2016), Guyanagarika represents the only known ECM genus
among the Agaricaleswith a distribution restricted to the Neo-
tropics, and more specifically to Guyana, based on current
knowledge and sampling. As only a small fraction of the esti-
mated fungal diversity is currently known (Blackwell 2011),
the knowledge of the distribution of this genus may be ex-
panded as new areas and more fungal taxa are studied.
Acknowledgements
This work was supported by a graduate research award from
the Department of Ecology and Evolutionary Biology at the
University of Tennessee to MSG; National Science Foundation
(NSF) DEB-0918591, DEB-1556412, and the National Geographic
Society’s Committee for Research and Exploration grants
6679-99, 7435-03 and 8481-08 to TWH; the Linnean Society of
London, the Explorers Club, and (NSF) DEB-1051782 to MCA;
and (NSF) DEB-1354802 to MES. Dillon Husbands functioned
as Guyanese local counterpart and assisted with field collect-
ing, descriptions, and specimen processing. Additional field
assistance in Guyana was provided by M. Chin, P. Henkel, C.
Andrew, V. Joseph, P. Joseph, F. Edmund, and L. Edmund. We
thank Rachel Swenie for her assistancewith the line drawings,
and the UT Genomics Core for providing sequencing services.
This paper is No. 223 in the Smithsonian Institution’s Biologi-
cal Diversity of the Guiana Shield Program publication series.
Appendix A. Supplementary data
Supplementary data related to this article can be found at
http://dx.doi.org/10.1016/j.funbio.2016.08.005.
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